Maintaining microbiome structure is critical for the health of both plants and animals. By re-screening a collection of Arabidopsis mutants affecting root immunity and hormone crosstalk, we identified a FERONIA (FER) receptor kinase mutant (fer-8) with a rhizosphere microbiome enriched in Pseudomonas fluorescens without phylum-level dysbiosis. Using microbiome transplant experiments, we found that the fer-8 microbiome was beneficial. The effect of FER on rhizosphere pseudomonads was largely independent of its immune scaffold function, role in development and jasmonic acid autoimmunity. We found that the fer-8 mutant has reduced basal levels of reactive oxygen species (ROS) in roots and that mutants deficient in NADPH oxidase showed elevated rhizosphere pseudomonads. The addition of RALF23 peptides, a FER ligand, was sufficient to enrich P. fluorescens. This work shows that FER-mediated ROS production regulates levels of beneficial pseudomonads in the rhizosphere microbiome.
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The microbiome sequencing data have been deposited in the National Center for Biotechnology Information BioProject database under accession PRJNA559927. The RNA-seq raw sequencing and analysed data have been deposited in the National Center for Biotechnology Information Gene Expression Omnibus database under accession GSE167143.
The code related to microbiome sequencing and RNA-seq analysis is available from the Haney laboratory GitHub repository (https://github.com/haneylab/).
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We thank F. M. Ausubel for critical reading of the manuscript and generous provision of the hsm mutant collection; A. Y. Cheung, Z. Y. Wang, X. Li, Y. Zhang and G. Wasteneys for kindly providing seed stocks; and the laboratory of M. Hirst for assistance with sequencing. This work was supported by an NSERC Discovery Grant (NSERC-RGPIN-2016-04121) and Weston Seeding Food Innovation grants awarded to C.H.H. Y.S. was supported by a kick-start award from the Michael Smith Laboratories (UBC) and a fellowship from the Chinese Postdoctoral Science Foundation. Early stages of this work were supported by NIH R37 grant GM48707 and NSF grants MCB-0519898 and IOS-0929226 awarded to F. Ausubel.
The authors declare no competing interests.
Peer review information Nature Plants thanks the anonymous reviewers for their contribution to the peer review of this work.
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Song, Y., Wilson, A.J., Zhang, XC. et al. FERONIA restricts Pseudomonas in the rhizosphere microbiome via regulation of reactive oxygen species. Nat. Plants 7, 644–654 (2021). https://doi.org/10.1038/s41477-021-00914-0
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